Influence of Apion sp. (, )SHORT stem-galls COMMUNICATION on induced resistance and leaf area of Diospyros hispida 433

Influence of Apion sp. (Brentidae, Apioninae) stem-galls on induced resistance and leaf area of Diospyros hispida (Ebenaceae)

Rodrigo A. de Souza1, Rafael Nessim2, Jean C. Santos3 & Geraldo Wilson Fernandes3,4

1Laboratório de Ecologia de Processos e Qualidade de Água, Departamento de Biologia Geral, Caixa Postal 486, ICB/Universidade Federal de Minas Gerais, 30161-970 Belo Horizonte-MG, Brasil. 2Ecologia de Populações, Departamento de Biologia Geral, Caixa Postal 486, ICB/Universidade Federal de Minas Gerais, 30161-970 Belo Horizonte-MG, Brasil. 3Ecologia Evolutiva & Biodiversidade/DBG, Caixa Postal 486, ICB/Universidade Federal de Minas Gerais, 30161-970 Belo Horizonte-MG, Brasil. 4Corresponding author

ABSTRACT. Influence of Apion sp. (Brentidae, Apioninae) stem-galls on induced resistance and leaf area of Diospyros hispida (Ebenaceae). We addressed the influence of the stem galls induced by an unidentified species of Apion – sensu lato (Brentidae, Apioninae) on the host plant, Diospyros hispida (Ebenaceae) leaf area and induced resistance against a Cecidomyiidae (Diptera) leaf galls. The study was performed in a cerrado vegetation in Serra do Cipó, southeastern Brazil. Although the number of leaves produced on galled and ungalled shoots did not differ statically (p>0.05), the presence of the apionid galls influenced the area of the leaves on the attacked shoots of D. hispida. Leaves on galled stems were approximately 50% smaller compared to leaves in healthy stems. The average of the cecidomyiid leaf galls successfully induced on healthy shoots was higher compared to galls successfully induced on shoots galled by the apionid. The same pattern was found for the abundance of hypersensitive reactions against the cedidomyiid gall induction. Therefore, the ability of the cecidomyiid to successfully induce galls was not influenced by the apionid galler.

KEYWORDS. Cecidomyiidae; Cerrado; hypersensitive reaction; galls; insect herbivory; Serra do Cipó.

RESUMO. Influencia das galhas caulinares de Apion sp. (Brentidae, Apioninae) sobre a resistencia induzida e área foliar de Diospyros hispida (Ebenaceae). Neste estudo verificamos a influência de galhas de ramos induzida por uma espécie não identificada de Apion sp. (Brentidae, Apioninae) sobre a área foliar da planta hospedeira Diospyros hispida (Ebenaceae) e na resistência induzida contra galhas de folhas de um Cecidomyiidae (Diptera). Este estudo foi conduzido em uma vegetação de cerrado na Serra do Cipó, sudeste do Brasil. Embora o número de folhas produzidas nos ramos galhados e não galhados não tenha diferido estaticamente (p>0,05), a presença das galhas de Apion sp. influenciou a área foliar nos ramos atacados de D. hispida. Folhas de ramos com galhas foram aproximadamente 50% menores quando comparadas a folhas em ramos saudáveis. A média de galhas foliares do Cecidomyiideae que se formaram com sucesso em folhas de ramos saudáveis foi maior quando comparado à média de galhas bem sucedidas em folhas de ramos galhados pelo Apion sp.. O mesmo padrão foi encontrado para a abundância de reações hipersensibilidade contra a formação de galhas do cecidomyiídeo. Portanto, a habilidade do cecidomyiídeo de induzir galhas não foi influenciada pelas galhas de Apion sp..

PALAVRAS-CHAVE. Cecidomyiidae; Cerrado; galhas de insetos; herbivoria por insetos; reação de hipersensibilidade; Serra do Cipó.

Gall induction by often act as physiological nutrient which the induced cells are readily found and killed. This sinks on their host plants, because nutrients move from mechanism has argued to be a hypersensitive response ungalled tissues and neighboring plant parts to the gall itself (Fernandes 1990, Fernandes et al. 2000). Through a series of (Kirst 1974, Larson & Whitham 1991). In addition to modify cascade morphological, biochemical and physiological events, the architecture of the attacked and neighboring host organs, the host plants elicit this induced-type of resistance, which galls may also affect the entire host plant (e.g. Mani 1964, terminates with the localization, confinement and death of the Hartnett & Abrahamson 1979, Fernandes 1987, Fernandes et attacked tissue (Fernandes et al. 2000, Fernandes & Negreiros al. 1999), thereby diminishing the performance of the host. 2001). Gall formation reduces flower, fruit, seed, and biomass Diospyros hispida DC. (Ebenaceae) is a woody shrub that production of several host plants (McCrea et al. 1985, Sacchi reaches two meters high and is found in the Cerrado (savanna) et al. 1988, Fernandes et al. 1993, Fernandes & Ribeiro 1990, and rupestrian fields of Brazil (Sano & Almeida 1998). In the Souza et al. 1998). cerrado of Serra do Cipó, in southeastern Brazil, this host In response to the feeding mode of galling insects, many species is attacked by two different species of galling insects. plant species evolved an elaborated defense mechanism by One of these galls is induced by an unidentified species of

Revista Brasileira de Entomologia 50(3): 433-435, setembro 2006 434 Souza et al.

Apion sp. (Araújo et al., 1995). Because some authorities have recently split the genus up (veja Alonzo-Zarazaga & Lyal 1999), we are uncertain which of the new genera our species belongs to. Hence, heretofore we refer to this species as Apion sp. – “sensu latu” (Brentidae: Apioninae) (see Kissinger 1968, see also Wibmer & O’brien (1986). The apionid attack new shoots inducing the growth of large galls which are globular, green and covered by a dense mat of short trichomes. Many galling larvae are found inside the galls that become brown and hard as they age. The second gall is induced by a still unidentified species of Cecidomyiidae (Diptera) (VC Maia, pess.com.) on the leaves of D. hispida. These galls are simple swellings on the leaf surface that have a discoid shape, are bright green, glabrous, and possess one chamber where only one larva is found. A Casual observations indicated that D. hispida elicits a hypersensitive reaction against the leaf galls induced by the cecidomyiid but not against the shoot galls. The reactions are observed as necrotic spots of rounded shape of reddish coloration on the leaf lamina on shoots with and without the apionid galls. The co-occurrence of apionid and cecidomyiid galls offers a scenario where we can observe whether the shoot galls influence the performance of the leaf galling cecidomyiid by evaluating Diospyros hispida’s ability to elicit the hypersensitive reaction to the leaf gall. Two questions were addressed in this study: Does the gall induced by the apionid affect the leaf area of attacked shoots? We postulated that as stem galls often deprives the terminal portion of attacked stems of nutrients and photosynthates (see Mani 1964, Souza et al. 1998), leaves would be smaller. How does the host plant B ability to elicit a hypersensitive response is influenced by the presence of shoot galls? We postulated that the abundance Fig. 1. (A) Healthy shoot; (B) apionid galls on shoot of Diospyros of cecidomyiid leaf galls would be higher on leaves on stems hispida (Ebenaceae). attacked by the apionid species, because these leaves would not be able to elicit the hypersensitive response fast enough in comparison to leaves on healthy stems (see Fernandes et al. 2000). whether the stem galls influenced the ability of the host plant The study was done in the Parque Nacional da Serra do in eliciting a hypersensitive response to the leaf galling Cipó (19°15’-1940’S, 43°30’- 43°55’W), Minas Gerais State, cecidomyiid, we counted all gall successfully formed and all Brazil, at 850 meters a.s.l. Diospyros hispida was found only hypersensitive reactions (galls found and killed by the plant) in a small area of disturbed cerrado vegetation (see Fernandes on leaves from both stem-galled and healthy shoots of D. 1994) of approximately 10,000 m2. In November of 2002 we hispida (see Fernandes & Negreiros 2001 for details). We then randomly selected 15 individuals of Diospyros hispida to used the t-test for dependent samples to compare the effect of answer the questions raised. From each individual plant we the shoot galls on leaf area and plants ability to elicit the randomly selected three pairs of galled shoots and their nearest hypersensitive reaction against the cecidomyiid galler. neighbor healthy shoots (without Apion sp. galls) to compare The number of leaves produced on shoots galled by the both the impact of the stem gall on leaf area, and stem gall apionid (5.7 ± 0.7, x ± SE) did not differ statistically from those effect on the leaf gall success. We counted all leaves present produced on ungalled shoots (6.4 ± 1.1, x ± SE, p = 0.39, n = on each shoot and then randomly collected three from each 30). On the other hand, shoots attacked by the apionid were shoot (n = 18 leaves per plant), numbered them according to clearly shorter than ungalled shoots. The presence of the the plant individual and presence of stem gall, placed in plastic apionid galls influenced the area of leaves on attacked stems bags and took them to the laboratory for further study. of D. hispida. Leaves on galled stems were approximately 50% To answer the question on the impact of the stem gall on smaller compared to leaves on healthy shoots. These results the leaf area of D. hispida, leaves of galled stems and healthy were expected as the apionid shoot galls are large and may stems were scanned on a digital scanner and the images induce a strong sink for plant photosynthates. Shoot galls are analyzed with the aid of the CIAS 2.0 program. To answer known to strongly influence the vascular bundles of the

Revista Brasileira de Entomologia 50(3): 433-435, setembro 2006 Influence of Apion sp. (Brentidae, Apioninae) stem-galls on induced resistance and leaf area of Diospyros hispida 435 attacked organ (Mani 1964). In many cases, they induce drastic (excepting Scolytidae and Platypodidae). Barcelona, changes in the architecture and performance of the attacked Entomopraxis, 315 p. Araújo, L. M.; A. C. F. Lara & G. W. Fernandes. 1995. Utilization of shoot, often causing their death (e.g. Silva et al. 1996, Souza Apion sp. (Coleoptera: Curculionidae) galls by an ant community in et al. 2001). southeastern Brazil. Tropical Zoology 8: 319–324. The number of cecidomyiid leaf galls successfully induced Fernandes, G. W. 1987. Gall forming insects: their economic importance on healthy shoots (29.3 ± 4.8, x ± SE, n = 15) was higher and control. Revista Brasileira de Entomologia 31: 379–398. Fernandes, G. W. 1990. 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Received 21/03/2006; accepted 25/08/2006

Revista Brasileira de Entomologia 50(3): 433-435, setembro 2006